Temperature-independent energy expenditure in early development of the African clawed frogXenopus laevis

Abstract

The thermal dissipation of activated eggs and embryos undergoing development from cleavage to the tailbud stage of the African clawed frog Xenopus laevis was measured as a function of incubation time at temperatures ranging from T = 288.2 K to 295.2 K, using a high-precision isothermal calorimeter. A23187-mediated activation of mature eggs induced stable periodic thermal oscillations lasting for 8-34 h. The frequency agreed well with the cell cycle frequency of initial cleavages at the identical temperature. In the developing embryo, energy metabolism switches from embryonic to adult features during gastrulation. The thermal dissipation after gastrulation fit well with a single modified Avrami equation, which has been used for modeling crystal-growth. Both the oscillation frequency of the activated egg and the growth rate of the embryo strongly depend on temperature with the same apparent activation energy of approximately 87 kJ mole(-1). This result suggests that early development proceeds as a single biological time, attributable to a single metabolic rate. A temperature-independent growth curve was derived by scaling the thermogram to the biological time, indicating that the amount of energy expenditure during each developmental stage is constant over the optimal temperature range.

Increasing demand for plasma membrane contributes to the energetic cost of early zebrafish embryogenesis

“…Xenopus leavis exhibits holoblastic cleavage divisions (meaning the yolk is contained within each of the cells), a similar slow exponential increase in heat dissipation has been observed (Nagano & Ode, 2014). Interestingly, the increase in heat dissipation slows down after cleavage and again after gastrulation during frog development (Nagano & Ode, 2014). These slow-downs coincide with the embryos mid-blastula transition and gastrulation during which the embryonic cell cycle lengthens by about 3fold and 8-fold respectively (Ferree, 2016;Siefert, 2015).…”

“…Xenopus leavis exhibits holoblastic cleavage divisions (meaning the yolk is contained within each of the cells), a similar slow exponential increase in heat dissipation has been observed (Nagano & Ode, 2014). Interestingly, the increase in heat dissipation slows down after cleavage and again after gastrulation during frog development (Nagano & Ode, 2014).…”

“…Thus, its metabolic and energetic profile that can be understood from basic principles, such as mass and energy conservation, stoichiometric constraints on production, homeostasis and morphometric parameter (Jusup, 2016). To investigate overall energetics, our lab has measured heat dissipation, which is equal to the net enthalpic change associated with all of the biochemical reactions taking place in the embryo (Rodenfels, 2019) The heat dissipated during the development of frog (Nagano & Ode, 2014), fish (Rodenfels, 2019) and fly (Song, 2019) embryos can be measured using isothermal calorimetry (ITC). The measurements show, for example, that embryogenesis is exothermic, meaning that the medium surrounding the embryos heats up.…”

Influence of temperature on reproduction and length of metamorphosis in Xenopus laevis (Amphibia: Anura)

“…It is thus readily adopted as an alternative experimental subject for developmental and cell biology (Figure 2). Nagano and Ode (2014) reported that the larvae of aquatic African clawed frogs were hatched within 2-3 days, and after losing the yellow follicle, they began to feed on algae suspended in the water column. Further, they found that the speed at which larvae hatch depends on ambient temperature.…”

“…Under optimal conditions, metamorphosis may be achieved within 2 months. The length of the conversion to a mature individual, depending on temperature and food, is approximately 6 to 8 weeks (Nagano & Ode 2014). Godfrey and Sanders (2004) found that Xenopus laevis embryo development is also significantly affected by water hardness and the concentrations of chlorine and salts.…”